Community Structure, Population Structure and Topographical Specialisation of Gyrodactylus (Monogenea) Ectoparasites Living On
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FOLIA PARASITOLOGICA 55: 187-196, 2008 Community structure, population structure and topographical specialisation ofGyrodactylus (Monogenea) ectoparasites living on sympatric stickleback species Joost A.M. Raeymaekers1, Tine Huyse1, Hannelore Maelfait12, Bart Hellemans1 and Filip A.M. Volckaert1 'Katholieke Universiteit Leuven, Laboratory of Animal Diversity and Systematics, Ch. Deberiotstraat 32, B-3000 Leuven, Belgium; 2Current address: Coordination Centre for Integrated Coastal Zone Management, Wandelaarkaai 7, B-8400 Oostende, Belgium Key words: host specificity, coexistence, Gasterosteus aculeatus, Pungitius pungitius, Gyrodactylidae, host density, site specificity, sympatry Abstract. In order to disentangle the contribution of host and parasite biology to host specificity, we compared the structure and population dynamics of the Gyrodactylus (von Nordmann, 1832) flatworm community living on sympatric three-spined Gasterosteus aculeatus L. and nine-spined Pungitius pungitius (L.) stickleback. Between April 2002 and March 2003, a small lowland creek was sampled monthly. Species identity of about 75% of the worms per host was determined with a genetic nu clear marker (ITS1). Each stickleback species hosted a characteristic gili- and fin-parasitic Gyrodactylus: G. arcuatus By- chowsky, 1933 and G. gasterostei Gläser, 1974 respectively infecting the three-spined stickleback, with G. rarus Wegener, 1910 and G. pungitii Malmberg, 1964 infecting the nine-spined stickleback. Host size and seasonal dynamics were strong determi nants of parasite abundance. A strong interaction between host and parasite species determined infection levels and affected three levels of parasite organisation: community structure, population structure and topographical specialisation. Community and population structure were shaped by asymmetric cross-infections, resulting in a net transmission of the Gyrodactylus species typical of the nine-spined stickleback towards the three-spined stickleback. Host density was not a major determinant of parasite exchange. Aggregation and topographical specialisation of the Gyrodactylus species of the three-spined stickleback were more pronounced than that of the nine-spined stickleback. The ecological context of the population dynamics of parasite community structure. For instance, specialist parasites is important to understand host-parasite sys parasite communities may reveal a higher degree of tems. Epidemiological models predict a positive rela nestedness than generalist parasite communities (Matë- tionship between host population density and abun jusová et al. 2000, Morand et al. 2002). Secondly, to dance of directly transmitted macroparasites (Ameberg pographical specialisation of ectoparasites may be in et al. 1998, Ameberg 2001). Variation in parasite abun fluenced by factors such as proximity to mates, compe dance may point to transmission rates relative to the tition, or host defence strategies (Reiczigel and Rózsa probability of physical contact between hosts. The 1998, ter Hofstede et al. 2004). population dynamics of directly transmitted parasites The link between ectoparasite ecology and host ecol may thus provide information on the interplay between ogy, and its consequences for parasite microhabitat, parasite population structure, parasite behaviour, host population and community structure seems evident, but ecology, and host behaviour. it is hard to disentangle the host and parasite component A central aspect of this interaction is host specificity, of host specificity in the field. Inference may be particu which determines whether a parasite is able to colonise larly strong when sympatric host species share a com a host (Sasal et al. 1999a). Host specificity can be munity of closely related, host-specific ectoparasites, strongly determined by host ecology, such as the degree accounting for several replications of host-parasite sys of host isolation, and by parasite ecology, such as mo tems in a single environment. The present study system bility (ter Hofstede et al. 2004). This is reflected in the consists of sympatric three-spined stickleback, parasite population structure. For instance, the degree of Gasterosteus aculeatus L., and nine-spined stickleback, physical contact between hosts affects the degree of Pungitius pungitius (L.). Both fishes host several mono- parasite aggregation (Sasal et al. 1999b). In ectopara genean parasites of the genus Gyrodactylus (von Nord sites, the host and parasite components of host specific mann, 1832) (Malmberg 1970, Dartnall 1973, Wootton ity may influence two additional levels of parasite or 1976, Cone and Wiles 1985, Harris 1985, Kalbe et al. ganisation. First, host specificity may account for ecto 2002, Özer et al. 2004). Gyrodactylus species are often Address for correspondence: J. Raeymaekers, Katholieke Universiteit Leuven, Laboratory of Animal Diversity and Systematics, Ch. Deberiot straat 32, B-3000 Leuven, Belgium. Phone: ++32 163 23 966; Fax: ++32 163 24 575; E-mail: [email protected] 187 highly specific (Harris 1985, Poulin 1992, Bakke et al. tory, each fish was measured (standard length, SL + 0.1 2002), and given their direct life cycle and direct trans cm), weighed (+ 0.01 g), inspected for Gyrodactylus sp. in a mission they are expected to depend heavily on host Petri-dish under a stereomicroscope, and dissected for sex biology. The stickleback immune system can respond determination when larger than 25 mm. All worms were strongly a few weeks after infection (Lester and Adams counted on each of the following fish body parts: caudal fin 1974, Raeymaekers et al. 2006). Although transmission (cf), anal fin (at), dorsal fin including spines (df), pelvic plate and pelvic spines (pf), left and right pectoral fin (pc), head by direct host contact is not the only route of transmis including the throat and the surface of the eyes (h), and the sion (Bakke et al. 1992, 2007), transmission rates are rest of the body (b) and gills (g). Gili covers were removed in probably correlated with the physical contact between order to dissect and inspect the gills. Detached worms were hosts (Boeger et al. 2005). counted separately. The three-spined and the nine-spined stickleback can Worms were collected with a dissection needle and trans coexist and are closely related, but their biology differs ferred to a 250 pi Eppendorf tube containing 5 pi Milli-Q considerably (Brâten 1966, Wootton 1976, 1984, Copp water. All worms were collected whenever possible. In case of and Kovác 2003, Hart 2003). The same is true for their high infection numbers, parasites were sampled proportionally Gyrodactylus species, which differ markedly in host to the distribution over the body, with a maximum of 50 specificity, microhabitat specificity and reproductive worms per fish. Eppendorf tubes were stored at -20°C until strategy, although the latter is less well understood further processing. Samples were digested by the addition of 5 (Harris 1993). Our first objective was to determine the pi of a double concentrated lysis solution, at a final concentra structure and seasonal dynamics of the Gyrodactylus tion of 1 X PCR buffer (Eurogentec), 0.45% Tween 20 communities and populations living on coexisting three- (Merck, Germany), 0.45% NP40 (Calbiochem, USA) and 60 and nine-spined sticklebacks. The occurrence of four pg E1 proteinase K (Sigma, USA). Tubes were centrifuged, Gyrodactylus species, identified with molecular tools, incubated at 65°C for 25 min, followed by incubation at 95°C for 10 min. was linked with host characteristics. Secondly, we stud Identification of the worms was based on the Internal Tran ied the site specificity of each Gyrodactylus species. scribed Spacer 1 (ITS1) rDNA region. The 20 pi PCR con Finally, three Gyrodactylus species in our study were tained 2 pi genomic DNA, 1 x PCR buffer (Eurogentec), 1.25 recorded on both stickleback species, with a higher oc mM MgCl2, 200 pM of dNTP, 1 pM ITS if (Cunningham currence on the “primary host” species compared to the 1997), 1 pM ITSlr (Zietara et al. 2002), 1 U of Silver Taq “secondary host” species. Ratios of infection success in Polymerase (Eurogentec) and Milli-Q water. Samples were primary versus secondary host species enabled us to subjected to an initial dénaturation step of 5 min at 95°C, fol compare the contribution of host and parasite compo lowed by 40 cycles of 30 s at 95°C, 30 s at 54°C and 30 s at nents to host specificity. We discuss the implications at 72°C, with a final elongation step of 7 min at 72°C. Aliquots three levels of parasite organisation: community struc (5 pi) of PCR products were run on a 1% agarose gel before ture, population structure, and topographical specialisa and after digestion with 5 U of restriction enzymes (RE). RE tion (sensu Pie et al. 2006). were selected based on all available ITS sequences from G. arcuatus Bychowsky, 1933, G. rarus Wegener, 1910, G. branchicus, Malmberg, 1964, G. pungitii Malmberg, 1964, MATERIALS AND METHODS and G. gasterostei Gläser, 1974 submitted to GenBank (AJ001839, AJ001841, AJ001845, AF156668, AF156669, AF Sampling and molecular identification. The study was 484543, AF328865, AF328867, AF328869, AY338442, carried out in a small eutrophic polder creek located in West- AY338443, AY338444, AY338445, AY061976). RE B st kerke (Belgium; 51°10’N, 3°00’E). The site is located near the 11071 was used to discriminate between G. gasterostei and G. North Sea coast, and has a very slow current of freshwater and